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On the EVOLUTION of SELF DURING the TRANSITION to MULTICELLULARITY 27 CHAPTER 2 THE EVOLUTION OF SELF DURING THE TRANSITION TO MULTICELLULARITY Aurora M. Nedelcu University of New Brunswick, Biology Department, Fredericton, New Brunswick, Canada Email: [email protected] Abstract: The notion of “self” is intrinsically linked to the concepts of identity and individuality. During evolutionary transitions in individuality—such as, for instance, during the origin of the first cell, the origin of the eukaryotic cell and the origin of multicellular individuals—new kinds of individuals emerged from the interaction of previously independent entities. The question discussed here is: How can new types of individuals with qualities that cannot be reduced to the properties of their parts be created at a higher level? This question is addressed in the context of the transition to multicellularity and using the volvocine green algae—a group of closely related unicellular and multicellular species with various degrees of physiological and reproductive unity—as a model system. In this chapter, we review our framework to addressing the evolution of individuality during the transition to multicellularity, focusing on the reorganization of general life‑traits and cellular processes and the cooption of environmentally‑induced responses. INTRODUCTION In philosophy, “self” is broadly defined as the essential qualities that make a person distinct from all others; the particular characteristics of the self determine its identity. The notion of “self” is, thus, intrinsically linked to the concepts of identity and individuality. Individuals are entities that are distinct in space and time. In biology, ©2012 Copyright Landes Bioscience and Springer. Not for Distribution ©2012 Copyright Landes Bioscience and Springer. individuals have been defined based on several additional criteria including genetic uniqueness, genetic homogeneity, or physiological autonomy.1 Going back to the root of the word individual (i.e., “not divisible”), individuals can also be thought of as the smallest units that cannot be divided into parts that maintain the essential properties of Self and Nonself, edited by Carlos López‑Larrea. ©2012 Landes Bioscience and Springer Science+Business Media. 14 THE EVOLUTION OF SELF DURING THE TRANSITION TO MULTICELLULARITY 15 the whole. Lastly, from an evolutionary perspective, individuals are units of selection that possess the properties of heritable variation in fitness.2 During evolutionary transitions in individuality—such as, for instance, during the origin of the first cell, the origin of the eukaryotic cell and the origin of multicellular individuals—new kinds of individuals emerged from the interaction of previously independent entities. Such associations can involve similar entities (such as during the transition to multicellularity) or rather distinct entities (such as during the evolution of the eukaryotic cell) and be based on a wide range of ecological interactions (from commensalism and mutualism to exploitation and parasitism; for discussion see ref. 3). The initial interactions can be facilitated by either aggregation (e.g., the formation of multicellular fruiting bodies in slime molds and myxobacteria) or the failure of offspring individuals to separate (which is the case during the development of most multicellular organisms). The long‑term stability of these associations and the subsequent integration of previously independent units into higher‑level individuals are dependent on the frequency of cooperative interactions and the mediation of the inherent conflicts among lower levels.3 At a mechanistic level, during transitions in individuality, a new genotype‑phenotype map has to be created to reflect the emergence of a new kind of individual (and a new “self”/identity) at the higher level. The way in which the lower‑level genotype‑phenotype maps are reorganized at the higher level can influence the potential for evolution of the newly emerged multilevel system.4 The question discussed here is: How can a new kind of individual with qualities that cannot be reduced to the properties of its parts be created at a higher level and how does this process affect the lower levels (i.e., the previously independent individuals) in terms of their own individualities and identities? We address this question in the context of the transition to multicellularity and using the volvocine green algae—a group of closely related unicellular and multicellular species with various degrees of physiological and reproductive unity—as a model system. For the purpose of this discussion, we define an individual as the smallest unit that is physiologically and reproductively autonomous. This definition restricts the term multicellular individual to organisms with two types of cells: reproductive (germ) cells and nonreproductive (somatic) sterile cells. In contrast to multicellular forms in which all cells have reproductive abilities—and thus each cell (part) can reproduce the group (the whole), in multicellular organisms with a germ‑soma separation, not all cells are able to recreate the whole; the evolution of nonreproductive cells renders the group indivisible and thus a true individual. We have approached the questions posed above from many perspectives: multilevel selection (in terms of cooperation, conflict and conflict mediation),3 fitness trade‑offs and fitness reorganization,2 life history trade‑offs,5 reorganization of general life‑traits and cellular processes4 and the cooption of environmentally‑induced responses.6 Below, we review our framework to addressing the evolution of individuality during the transition to multicellularity, focusing on the two latter perspectives. Specifically, we Not for Distribution ©2012 Copyright Landes Bioscience and Springer. have argued that the emergence of individuality at a higher level (and the emergence of a new genotype‑phenotype map) requires (i) the dissociation of certain processes, traits and functions at the lower level and their reorganization at the higher level, (ii) the cooption of lower‑level processes and pathways for new functions at the higher level and (iii) changes in gene expression patterns, from a temporal into a spatial context.4,6,7 We have also suggested that some of the differences among extant multicellular lineages (including differences in their evolutionary potential) can be explained by the way in which the reorganization of these processes and traits (and the emergence of the new 16 SELF AND NONSELF genotype‑phenotype map) has been achieved during the transition to multicellularity and the evolution of individuality at the higher level.4 Volvocine algae exemplify well these suggestions. In this group, the transition to multicellularity embraced unique paths, partly due to the constraints inherited from their unicellular ancestors. THE VOLVOCINE ALGAE AS A CASE STUDY “Few groups of organisms hold such a fascination for evolutionary biologists as the Volvocales. It is almost as if these algae were designed to exemplify the process of evolution”.8 Diversity Volvocine algae are photosynthetic biflagellated green algae in the order Volvocales, comprising closely related unicellular (Chlamydomonas‑like) and multicellular forms that show a progressive increase in cell number, volume of extracellular matrix per cell, division of labor and ratios between somatic and reproductive cells9 (Fig. 1). Interestingly, somatic cell specialization and higher‑level individuality evolved multiple times in this group and the different levels of complexity are thought to represent alternative stable states (among which evolutionary transitions have occurred several times during the evolutionary history of the group), rather than a monophyletic progression in organizational and developmental complexity.9,10 The observed morphological and developmental diversity among volvocine algae appears to result from the interaction of conflicting structural and functional constraints and strong selective pressures. CONSTRAINTS All volvocine algae share the so‑called “flagellation constraint”,11 which has a different structural basis than the one invoked in the origin of metazoans.12 Specifically, in volvocine algae, because of their coherent rigid cell wall the position of flagella is fixed and thus, the basal bodies cannot move laterally and take the position expected for centrioles during cell division while still remaining attached to the flagella (as they do in “naked”, wall‑less green flagellates). Therefore, cell division and motility can take place simultaneously only for as long as flagella can beat without having the basal bodies attached (i.e., only up to five cell divisions). The presence of a coherent cell wall is coupled with the second conserved feature among volvocine algae—namely, their unique way of cell division. In this green algal group, cells do not double in size and then undergo binary fission. Rather, each cell Not for Distribution ©2012 Copyright Landes Bioscience and Springer. grows about 2n‑fold in volume, followed by a rapid, synchronous series of n divisions under the mother cell wall; this type of cell division is referred as to multiple fission or palintomy (i.e., the process during which a giant parental cell undergoes a rapid sequence of repeated divisions, without intervening growth, to produce numerous small cells). Because clusters, rather than individual cells, are produced in this way, this type of division was suggested to have been an important precondition facilitating the THE EVOLUTION OF SELF DURING THE TRANSITION TO MULTICELLULARITY
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